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Genome Analysis, Metabolic Potential, and Predatory Capabilities of Herpetosiphon llansteffanense sp. nov.

ABSTRACT: Herpetosiphon spp. are ubiquitous, chemoheterotrophic, filamentous gliding bacteria with the ability to prey on other microbes through a "wolf pack" mechanism. The genus currently comprises four known species (H. aurantiacus, H. geysericola, H. giganteus, and H. gulosus), which produce antimicrobial secondary metabolites such as siphonazole. As part of a study isolating myxobacterial wolf pack predators, we serendipitously isolated a novel environmental strain (CA052B) from the edge of a stream at Llansteffan, United Kingdom, which was identified as a member of the Herpetosiphon genus. A lawn culture method was utilized to analyze the predatory activity of CA052B against 10 prey organisms of clinical relevance. CA052B was found to prey on Escherichia coli, Klebsiella pneumoniae, Proteus mirabilis, Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus saprophyticus, Enterococcus faecalis, Bacillus subtilis, and Candida albicans Purified CA052B outer membrane vesicles also exhibited killing activity against the prey organisms when tested by flow cytometry. 16S rRNA sequencing of CA052B showed 98 to 99% identity with other Herpetosiphon species members. Comparing the genome of CA052B with the publicly available genomes of H. aurantiacus and H. geysericola revealed average nucleotide identities of only 84% and 91%, respectively, whereas the genome-to-genome distance calculation showed sequence identities of 28.2% and 46.6%, respectively. Biochemical characterization also revealed distinctions between CA052B and both H. gulosus and H. giganteus Thus, strain CA052B^T (= DSM 107618^T = NBRC 113495^T) is proposed to be the type strain of a novel species, Herpetosiphon llansteffanense sp. nov. The genome sequence of CA052B also revealed diverse secondary metabolite biosynthetic clusters, encouraging further exploration of its antibiotic production potential.IMPORTANCE Predatory bacteria are able to kill and consume other microbes and are therefore of interest as potential sources of new antimicrobial substances for applications in the clinic. "Wolf pack" predators kill prey by secreting antimicrobial substances into their surroundings, and those substances can kill prey organisms independently of the predatory cells. The genus Herpetosiphon exhibits wolf pack predation, yet its members are poorly described compared to other wolf pack predators, such as the myxobacteria. By providing a thorough characterization of a novel Herpetosiphon species, including its predatory, biochemical, and genomic features, this study increases our understanding of genomic variation within the Herpetosiphon genus and how that variation affects predatory activity. This will facilitate future rational exploitation of genus members (and other wolf pack predators) as sources of novel antimicrobials.

SUBMITTER: Livingstone PG

PROVIDER: S-EPMC6210107 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Corallococcus spp. are common soil-dwelling organisms which kill and consume prey microbes through the secretion of antimicrobial substances. Two species of Corallococcus have been described previously (Corallococcus coralloides and Corallococcus exiguus). A polyphasic approach, including biochemical analysis of fatty acid methyl esters, substrate utilization, and sugar assimilation assays, was taken to characterize eight Corallococcus species strains and the two type strains. The genomes of all strains, including that of C. exiguus DSM 14696T (newly reported here), shared an average nucleotide identity below 95% and digital DNA-DNA hybridization scores of less than 70%, indicating that they belong to distinct species. In addition, we characterized the prey range and antibiotic resistance profile of each strain, illustrating the diversity of antimicrobial activity and, thus, the potential for drug discovery within the Corallococcus genus. Each strain gave a distinct profile of properties, which together with their genomic differences supports the proposal of the eight candidate strains as novel species. The eight candidates are as follows: Corallococcus exercitus sp. nov. (AB043AT = DSM 108849T = NBRC 113887T), Corallococcus interemptor sp. nov. (AB047AT = DSM 108843T = NBRC 113888T), Corallococcus aberystwythensis sp. nov. (AB050AT = DSM 108846T = NBRC 114019T), Corallococcus praedator sp. nov. (CA031BT = DSM 108841T = NBRC 113889T), Corallococcus sicarius sp. nov. (CA040BT = DSM 108850T = NBRC 113890T), Corallococcus carmarthensis sp. nov. (CA043DT = DSM 108842T = NBRC 113891T), Corallococcus llansteffanensis sp. nov. (CA051BT = DSM 108844T = NBRC 114100T), and Corallococcus terminator sp. nov. (CA054AT = DSM 108848T = NBRC 113892T).IMPORTANCE Corallococcus is a genus of predators with broad prey ranges, whose genomes contain large numbers of gene clusters for secondary metabolite biosynthesis. The physiology and evolutionary heritage of eight Corallococcus species strains were characterized using a range of analyses and assays. Multiple metrics confirmed that each strain belonged to a novel species within the Corallococcus genus. The strains exhibited distinct patterns of drug resistance and predatory activity, which mirrored their possession of diverse sets of biosynthetic genes. The breadth of antimicrobial activities observed within the Corallococcus genus highlights their potential for drug discovery and suggests a previous underestimation of both their taxonomic diversity and biotechnological potential. Taxonomic assignment of environmental isolates to novel species allows us to begin to characterize the diversity and evolution of members of this bacterial genus with potential biotechnological importance, guiding future bioprospecting efforts for novel biologically active metabolites and antimicrobials.

Project description:A novel bacterial strain, designated YN101T, was isolated from a marine solar saltern in the coast of Weihai, Shandong Province, China. Strain YN101T was Gram-stain negative, facultatively anaerobic, oxidase and catalase negative bacterium with the ability to prey on other microbes. A cross-streaking culture method was utilized to analyze the predatory activity of strain YN101T. The results showed strain YN101T could prey on various bacteria, either Gram-stain negative or Gram-stain positive. According to the predatory assays, different species in the same genus may behave differently when attacked by strain YN101T. The predatory behavior of strain YN101T to four typical species was analyzed, and furthermore, predation to Algoriphagus marinus am2T were quantitatively studied by fluorogenic quantitative PCR, and the gene copies decreased over two magnitudes. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strain YN101T shared the greatest sequence similarity of 93.9% to Bradymonas sediminis FA350T. The complete genome sequence of strain YN101T was 8,047,306 bp in size and the genomic DNA G + C content was 63.8 mol%. The digital DNA-DNA hybridization (dDDH) values and average nucleotide identity (ANI) values between strain YN101T and B. sediminis FA350T were 13.9 and 74.0%. The genetic features showed that the biosynthesis of many important compounds was deficient in genome of strain YN101T, which may lead to its predation. Moreover, its genome encoded many genes affiliated with type IV pili, secretion system, membrane proteins and transduction proteins. Similar with myxobacteria and Bdellovibrio and like organisms (BALOs), these genes should play important roles in motility, adhesion or virulence to attack prey cells during predation. The predominant polar lipid profile of strain YN101T consisted of phosphatidylethanolamine (PE), phosphatidylglycerol (PG), diphosphatidylglycerol (DPG), and one unidentified aminophospholipid (APL). The major cellular fatty acid of strain YN101T was iso-C17:0, and the sole respiratory quinone was MK-7. Based on the chemotaxonomic, physiological and biochemical characteristics, strain YN101T represents a novel species of a novel genus in the family Bradymonadaceae, for which the name Persicimonas caeni gen. nov., sp. nov. is proposed. The type strain is YN101T (=KCTC 72083T = MCCC 1H00374T).

Project description:BackgroundThe phylum Bacteroidota represents a significant proportion of heterotrophic bacteria found in marine ecosystems. Members of the phylum Bacteroidota are actively involved in the degradation of biopolymers such as polysaccharides and proteins. Bacteroidota genomes exhibit a significant enrichment of various enzymes, including carbohydrate-active enzymes (CAZymes), carboxypeptidases, esterases, isomerases, peptidases, phosphatases, and sulfatases. The genus Marivirga, a member of the family Marivirgaceae within the phylum Bacteroidota, comprises six documented species. During a microbial diversity study, three novel Marivirga strains (BKB1-2 T, ABR2-2, and BDSF4-3 T) were isolated from the West Sea, Republic of Korea.ResultsTo explore the taxonomic status and genomic characteristics of the novel isolates, we employed a polyphasic taxonomic approach, which included phylogenetic, chemotaxonomic and comprehensive genome analysis. The three isolates were Gram-stain-negative, aerobic, rod-shaped, moderately halophilic, and had a gliding motility. The average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values among the two isolates, BKB1-2 T and BDSF4-3 T, and the six reference strains were 70.5-76.5% for ANI and 18.1-25.7% for dDDH. Interestingly, the Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that the strains harbor genes for a comprehensive pathway for dissimilatory nitrate reduction to ammonium (DNRA), as well as other nitrogen pathways for the reduction of nitrite, nitric oxide, and nitrous oxide. Additionally, the antiSMASH analysis indicated that the strains contained three to eight biosynthetic gene clusters (BGCs) associated with the synthesis of secondary metabolites. Furthermore, the strains carried a high number of CAZyme ranging from 53 to 152, which was also demonstrated by an in vitro analysis of degradation of the polysaccharide cellulose, chitin, laminarin, starch, and xylan. Additionally, all the strains carried genes for the metabolism of heavy metals, and exhibited tolerance to heavy metals, with minimum inhibitory concentrations (MICs) in millimoles (mM) in ranges of Co2+ (3-6), Cu2+ (0.2-0.4), Ni2+ (3-5), Zn2+ (2-4), Mn2+ (20-50), and Hg2+ (0.3).ConclusionsBased on polyphasic taxonomic approach, the three isolated strains represent two novel species names Marivirga arenosa sp. nov. (BKB1-2 T = KCTC 82989 T = InaCC B1618T), and Marivirga salinae sp. nov. (BDSF4-3 T = KCTC 82973 T = InaCC B1619T).

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Genome Analysis, Metabolic Potential, and Predatory Capabilities of Herpetosiphon llansteffanense sp. nov.

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